ORIGINAL RESEARCH SPINE

Spinal Cord Injury after Blunt Cervical Spine Trauma: Correlation of Soft-Tissue Damage and Extension of Lesion

R. Martínez-Pe´rez, I. Paredes, S. Cepeda, A. Ramos, A.M. Castan˜o-Leo´n, C. García-Fuentes, R.D. Lobato, P.A. Go´mez, and A. Lagares

ABSTRACT BACKGROUND AND PURPOSE: In patients with spinal cord injury after blunt trauma, several studies have observed a correlation between neurologic impairment and radiologic findings. Few studies have been performed to correlate spinal cord injury with ligamentous injury. The purpose of this study was to retrospectively evaluate whether ligamentous injury or disk disruption after spinal cord injury correlates with lesion length.

MATERIALS AND METHODS: We retrospectively reviewed 108 patients diagnosed with traumatic spinal cord injury after cervical trauma between 1990–2011. Plain films, CT, and MR imaging were performed on patients and then reviewed for this study. MR imaging was performed within 96 hours after cervical trauma for all patients. Data regarding ligamentous injury, disk injury, and the extent of the spinal cord injury were collected from an adequate number of MR images. We evaluated anterior longitudinal ligaments, posterior longitudinal ligaments, and the ligamentum flavum. Length of lesion, disk disruption, and ligamentous injury association, as well as the extent of the spinal cord injury were statistically assessed by means of univariate analysis, with the use of nonparametric tests and multivariate analysis along with linear regression.

RESULTS: There were significant differences in lesion length on T2-weighted images for anterior longitudinal ligaments, posterior longi- tudinal ligaments, and ligamentum flavum in the univariate analysis; however, when this was adjusted by age, level of injury, sex, and disruption of the soft tissue evaluated (disk, anterior longitudinal ligaments, posterior longitudinal ligaments, and ligamentum flavum) in a multivariable analysis, only ligamentum flavum showed a statistically significant association with lesion length. Furthermore, the number of ligaments affected had a positive correlation with the extension of the lesion.

CONCLUSIONS: In cervical spine trauma, a specific pattern of ligamentous injury correlates with the length of the spinal cord lesion in MR imaging studies. Ligamentous injury detected by MR imaging is not a dynamic finding; thus it proved to be useful in predicting neurologic outcome in patients for whom the MR imaging examination was delayed.

ABREVIATIONS: ALL ϭ anterior longitudinal ligament; ASIA ϭ American Spinal Injury Association Impairment Scale; LF ϭ ligamentum flavum; PLL ϭ posterior longitudinal ligament; SCI ϭ spinal cord injury; SCIWORA ϭ spinal cord injury without radiological abnormalities

cute traumatic spinal cord injury (SCI) is located at the cer- for patients with acute cervical spine injury.3 Since the early 1990s, Avical level in 45–75% of cases.1,2 Thus, cervical trauma is several studies have investigated the role of several radiologic potentially the source of long-term disability because of its asso- findings in SCI.3,4 Previous published reports have described ciated risk of SCI.2 The internal architecture of the spinal cord, as the mechanism and biomechanics of spinal stability after blunt well as soft tissue injury, is best visualized with MR imaging. How- trauma.5-7 It is believed that the degree of soft-tissue damage is ever, MR imaging performed after the cervical trauma has prog- related to the severity of the SCI. However, very few studies have nostic implications for the therapeutic management of this dis- similarly shown this association. ease; hence, it has become part of the standard imaging protocol Instead, the correlation between lesion length and neurologic outcome has been sufficiently demonstrated in the acute phase 8,9 Received February 5, 2013; accepted after revision September 9. after cervical trauma. In fact, it has been recommended that the 10 From the Departments of Neurosurgery (R.M.-P., I.P., S.C., AM.C.-L., R.D.L., P.A.G., first MR imaging should be performed 24–72 hours after injury. A.L.) and Radiology (A.R.), and Intensive Care Unit (C.G.-F.), Hospital 12 de Octubre, The prognostic value of MR imaging in later stages is less clear Universidad Complutense de Madrid, Madrid, Spain. Please address correspondence to Rafael Martı´nez-Pe´rez, MD, Hospital 12 de Oc- because of the dynamic nature of edema and the dependence on tubre. Andalucía s/n, 28041, Madrid, Spain; e-mail: rafa11safi[email protected] the lesion length after trauma.11 Therefore, we designed this study http://dx.doi.org/10.3174/ajnr.A3812 to detect soft-tissue injuries that are related to more pronounced

AJNR Am J Neuroradiol 35:1029–34 May 2014 www.ajnr.org 1029 FIGURE. A, Traumatic herniation disk producing spinal cord compression at the same level; it is seen as hyperintensity in the T2-weighted image. Lesion length is measured in millimeters from the most cephalad level to the lowest (arrows). B, Sagittal projection on T2-weigthed images. Disruption of posterior longitudinal ligament is visualized at level C5–C6. C, Sagittal projection on T2-weighted image. At level C7–T1, the injured anterior longitudinal ligament (arrow) is seen. Signal changes are shown at level C6–C7. D, Damage in anterior longitudinal ligament, posterior longitudinal ligament, ligamentum flavum, and disk are represented by a disruption in low signal intensity corresponding to this structure. lesions, which MR imaging can detect, including more severe SCI. Table 1: American Spinal Injury Association Impairment Scale Soft-tissue injury is a more static finding than is cord edema and Grade A Complete: No sensory or motor function is can convey potentially relevant information when MR imaging is preserved in the sacral segments S4–S5 delayed (Fig 1). Grade B Incomplete: Sensory but not motor function is preserved below the neurological level and includes the sacral segments S4–S5 MATERIALS AND METHODS Grade C Incomplete: Motor function is preserved below the Patients with known SCI after non-penetrating cervical spine neurological level, and more than half of key trauma over a 21-year period were recruited in the clinical, retro- muscles below the neurological level have a spective data base. Only patients in whom cervical MR imaging muscle grade Ͻ3 was performed within 96 hours after trauma were selected for Grade D Incomplete: Motor function is preserved below the neurological level, and at least half of key further analysis. muscles below the neurological level have a Patients who were neurologically intact, or whose MR imaging muscle grade Ն3 was performed after the fourth day of the injury, were excluded. Grade E Normal: Sensory and motor function is normal Patients with severe traumatic brain injury or upper cervical spine injuries (C1–C2 fractures) were also excluded from the analysis. Thoracic injuries were not included either. analyzed with anterior longitudinal ligament (ALL), posterior We recorded clinical variables, including age, sex, mechanism longitudinal ligament (PLL), and ligamentum flavum (LF), and of injury, and neurologic status. Epidemiologic data also exam- the intervertebral disk was examined. In all patients, MR imaging ined age, sex, and mechanism of injury from the medical records. was performed within the first 4 days after trauma. MR imaging Neurologic status was assessed clinically during the first examina- was performed with the use of a 1.5T magnet and 3-mm section tion by using the American Spinal Injury Association Impairment thickness for axial and sagittal planes. We analyzed ligamentous Scale (ASIA) (Table 1). injury by assessing disruption in T1- and T2-weighted images (in Plain radiographs, CT scans, and MR images were consensu- a sagittal plane), including axial T2- and T2*-weighted images. In ally assessed by a neurosurgeon trained in cervical trauma images all patients, lesion length was determined by intramedullary cord (I.P.) and an experimental neuroradiologist (A.R.). Both observ- signal intensity change in T2-weighted images and was defined as ers were blinded to patient clinical and neurologic data. the distance in millimeters between the most caudal and cephalad To diagnose the level and extension of injury and determine signal intensity change in the cord. Soft-tissue disruption was de- the number of fractures, plain radiographs, MR imaging, and CT fined as a clear MR imaging signal with complete discontinuity of were used. The presence of fracture and bone integrity was as- the structure in all appropriate imaging sections. sessed in the CT scan. The segment affected was defined as fracture level with only 1 Soft-tissue injury was assessed with the use of MR imaging and fracture: if there was more than 1, it was defined as the fracture 1030 Martínez-Pe´rez May 2014 www.ajnr.org level that produced the most cord compression. In cases with SCI Table 2: Characteristics of patients with acute traumatic cervical but without radiologic abnormalities (SCIWORA), we consid- SCI ered the segment to be affected when the soft tissues were most Characteristic No. of Patients (%) injured. Mean age, y 40.5 (17–86) Male 87 (80.6) We analyzed the data with univariate and multivariate meth- Female 21 (19.4) ods to compare the damage of soft-tissue structures (LF, ALL, Severity of SCI PLL, and disk), including the extent of SCI. ALL, PLL, LF, and disk ASIA A 39 (36.1) injuries were independently analyzed as dichotomous variables ASIA B 10 (9.3) ASIA C 22 (20.3) (damaged or intact); the extent of SCI (distance between the most ASIA D 37 (34.3) caudal and cephalad of the cord signal intensity change [hyperin- Spinal level of SCI tensity] in a sagittal plane, T2-weighted image measured in milli- C3–C4 16 (14.8) meters) was considered to be a continuous variable. Levels of C4–C5 22 (20.3) injury, age, and sex were analyzed as potential covariates. Sex C5–C6 31 (28.7) C6–C7 24 (22.2) (male/female) and level of injury (upper lesion, C3-C4-C5 and C7–T1 15 (13.8) lower lesion, C6-C7-C8) were considered dichotomous variables, Cause of SCI whereas age was seen as a continuous variable. The Mann-Whit- Motor vehicle crash 61 (56.4) ney U test compared lesion length of each predefined qualitative Car crash 35 (32.4) variable (ALL, PLL, LF, and disk damage, sex, and level of injury). Pedestrians 8 (7.4) Motorcyclists 18 (16.6) Spearman ␳ was calculated to demonstrate the correlation be- Falls 33 (30.6) Ͻ tween lesion length and age. Variables with a value of P .1 were Sport injury 9 (8.3) included in the multivariate analysis. Linear regression was used Aggression/assault 5 (4.6) for the multivariate analysis as well. The Kruskall-Wallis test could also probe a possible associa- Table 3: Univariate analysis: Qualitative variables (soft tissues) tion between how many ligaments were affected (none, 1, 2, or 3 Mean Length of ligaments), including lesion length. No. of Cases (%) Lesion, mm P The association between lesion length and neurologic status Structure Intact Disrupted Intact Disrupted Value was also analyzed. Lesion length was considered a continuous ALL 51 (47.2) 57 (52.8) 43.22 64.60 Ͻ.001 variable, as stated previously. Neurologic status at admission was PLL 45 (41.7) 63 (58.3) 47.64 59.40 .05 separated as complete SCI (ASIA A) and incomplete SCI (ASIA B, LF 56 (51.9) 52 (48.1) 35.96 74.46 Ͻ.001 C, and D). We used a t test to compare the lesion length for the 2 Disk 46 (42.6) 62 (57.4) 47.48 59.71 .044 groups. The threshold for statistical significance was P Ͻ .05, and all tests were calculated by use of SPSS v20 (IBM, Armonk, New Table 4: Multivariate analysis: Linear regression York). Dependent Variable Independent Variable P Value Lesion length (mm) ALL .395 PLL .525 RESULTS LF Ͻ.001 We retrospectively reviewed 331 patients with known or sus- Disk .464 pected SCI or with radiculopathy after a non-penetrating cervical Age .215 spine trauma who presented to the emergency department or the Note:—R2 value of prediction model number 1 ϭ 0.365. intensive care unit at our institution between 1990–2011. MR imaging was performed on 186 patients within 96 hours after Age was correlated with lesion length (P ϭ .036) in the univar- trauma who were then selected for further analysis. We excluded iate analysis and was included in the multivariate analysis as a 40 patients with severe traumatic brain injury from the analysis. covariate. The level of lesion (P ϭ .449) and sex (P ϭ .398) were In addition, 38 patients with upper cervical spine trauma (C1–C2 not associated with larger lesions in the univariate analysis. Eigh- fractures) were also excluded. Finally, data analysis included 108 teen patients did not show hyperintensity changes in T2-weighted patients (87 men and 21 women, ages 17–86 years; overall mean images. ALL was disrupted in 52.8% of cases, PLL in 58.3%, LF in age, 40.5 years) (Table 2). Seventy-four patients had 1 fracture, 13 48.1%, and disk in 57.4%. Average cord lesion length (in mm) for patients had 2, and 3 patients had 3 noncontiguous fractures, disrupted and non-disrupted soft tissue was 64.60 and 43.22 for respectively. In 18 patients, there was no evidence of any fracture ALL, 59.40 and 47.64 for PLL, 74.46 and 35.96 for LF, 59.71 and after radiologic examination: all patients were diagnosed with SCI 47.48 for disk, respectively. All structures showed a greater mean without radiologic abnormalities (SCIWORA). The most com- lesion length when there was soft-tissue disruption, compared mon mechanism of injury was motor vehicle crash (Table 2). The with when there was not disruption. With the use of univariate C5–C6 spinal level was most commonly involved (Table 2). As analysis, LLA, PLL, LF, and disk disruption were related to a stated, MR imaging was performed within 96 hours after the significantly larger lesion length (Table 3). However, in multi- trauma occurred in all patients, whereas in 81.4% of these pa- variate analysis, LF was the only structure showing a significant tients, it was performed within the first 72 hours. According to association between the ligament injured and greater lesion ASIA, there were 39 patients with ASIA A, 10 patients with ASIA length (Table 4). B, 22 patients with ASIA C, and 37 patients with ASIA D (Table 2). There were 22 patients without disrupted ligaments, 34 with 1 AJNR Am J Neuroradiol 35:1029–34 May 2014 www.ajnr.org 1031 disrupted ligament, 17 with 2 disrupted ligaments, and 35 with 3 as measured in T2-weighted images; when this was adjusted for disrupted ligaments. Mean lesion lengths in millimeters were age, level of injury, sex, and ligamentous or disk injury in a mul- 29.75, 50.15, 56.38, and 73.37 for none, 1, 2, and 3 disrupted tivariate analysis, only LF injury was found to be significantly ligaments, respectively. The number of disrupted ligaments cor- associated with lesion length. related with lesion length (Pearson correlation coefficient, 0.49; We hypothesize that LF injury is more strongly correlated with P Ͻ .01). extension of cord damage, in that posterior elements are associ- Patients with complete SCI at admission had a larger in- ated with increased instability and therefore with greater SCI. An- tramedullary lesion (P Ͻ .001) than did patients with incomplete other possible explanation is that the LF is more elastic and that SCI. more pressure is needed to break it. The force required for this kind of injury would be responsible for SCI; it is probably the DISCUSSION result of a combination of the 2 mechanisms because they are not Previous studies show that lesion lengths measured in sagittal mutually exclusive. We excluded patients with upper cervical T2-weighted images are related to patient prognosis.9,12-14 Edema fractures because these lesions are the result of different injury is seen in T2 MR imaging sequences as hyperintensity of the signal mechanisms.18 within the cord, whereas a low intensity area on T2-weighted im- Several prognostic factors have been described as predictive of ages in the acute stage is thought to indicate intramedullary hem- traumatic spinal cord damage.10,13,17,29-32 Some studies have fo- orrhage, attributed to deoxyhemoglobin.15,16 In addition, be- cused on particular clinical features, such as SCIWORA,29,33 Cen- cause hemorrhage is almost always concurrent with edema, it is tral Cord syndrome,29 or Brown-Sequard syndrome.34 Evidence common to measure signal hyperintensity in T2-weighted images in the literature shows that more severe abnormalities seen to determine the length of the lesion.17 It is not clear whether these through MR imaging have been associated with more severe neu- signal changes are a result of primary or secondary spinal cord rologic status. Excessive edema, changes in T2-weighted images, damage.18 greater degree of cord compression, and hemorrhage have been MR imaging may be a useful tool in the management of cervi- related to worse neurologic outcomes.9,35-38 Gain in motor cal trauma, especially in cases of questionable structural instabil- strength at follow-up has been seen to correlate with a decrease in ity, because it is extremely useful in detecting soft-tissue in- T2-weighted hyperintensity in serial MR imaging studies.39 Some jury.19,20 Patients without demonstrated abnormalities in plain authors have described a close correlation between level of injury radiographs or CT may show signs of instability with MR imag- and severity of SCI.30 Miranda et al34 found an association be- ing, as determined by soft-tissue involvement. Some authors have tween MR imaging signal changes and level of injury. Therefore, demonstrated that different ligamentous injuries are associated because the level of injury is related anatomically with the level of with spinal instability; therefore, this could serve as a guide for fracture, we also introduced this factor in the multivariate analy- surgical treatment of traumatic instability of the spinal cord. sis. To our knowledge, there is 1 paper in the literature that relates Greater posterior vertebral body translation and angulation are the severity of ligamentous injury with degree of SCI.6 In this related to disruption of the posterior ligamentous complex21,22 study, we found that the severity of PLL, versus ALL injury, was and are indirect signs of spinal instability. correlated with more severe SCI, especially in patients with exten- For assessing disruption of ligaments, T2-weighted images in sion fractures. the sagittal plane should be included in all MR imaging proto- Our study found that patients without signal changes in the cols.3 Other sequences have been described in the literature to spinal cord had few neurologic deficits. Patients with complete rule out soft-tissue injuries, such as fat-suppressed T2 images SCI showed larger lesions than did those with incomplete SCI. (STIR).19,20 In acute cervical trauma, MR imaging has moderate This in turn highlights the correlation between radiologic and to high sensitivity for injury of specific ligamentous structures but clinical findings. low specificity for intraoperative findings of the same injuries.23,24 The posterior ligamentous complex consists of supraspinous and Limitations interspinous ligaments: the LF, the facet capsules, and the cervical The first limitation of our study may be related to the timing of the fascia.25-28 In several studies, MR imaging was also sensitive for MR imaging. Clinical instability associated with cervical trauma the evaluation of injury of the posterior ligamentous com- sometimes impedes the reliability of MR imaging in the first plex19,24; this suggests that injury to ALL may be underestimated hours. A review of the literature by Bozzo et al3 concluded that with the use of MR imaging, if the findings are considered in MR imaging should be done in the acute period after SCI for isolation. The explanation is that ALL and PLL adhere to the disk, better prognostication. It has also been recommended that the whereas only the ALL adheres to the vertebrae, such that the PLL first MR imaging should be performed 24–72 hours after is easier to identify.3 trauma.10 However, there is a lack of evidence supporting precise We have discussed the importance of MR imaging in the de- guidelines.3,23 In fact, transferring critical or unstable patients tection of ligamentous injury after cervical trauma: it also deter- from the intensive care unit to an x-ray room presents an unac- mines the structural stability of the cervical spine. Spinal instabil- ceptable risk during the first days, especially in patients with ity is related to neurologic injury and therefore to cord injury trauma. Length of edema in T2-weighted images depends on the because the involvement of soft tissue may play a role in the extent time when the MR imaging was performed after trauma.11 The of SCI. This report shows that damage to soft tissue such as LF, extension of the lesion may be overestimated in patients in whom ALL, PLL, and disk is related to longer-length cord hyperintensity MR imaging was performed at a later point in time. To focus on 1032 Martínez-Pe´rez May 2014 www.ajnr.org acute traumatic injury, and to minimize potential bias introduced intramedullary signal changes are dynamic, and their prognostic with chronic injury, we only included patients who had under- value decreases over time. Injury of the LF is a feature perdurable gone MR imaging during the first 96 hours after injury. In 82.4% over time. It can also be detected when MR imaging is performed of these patients, MR imaging was performed within 72 hours at a more delayed stage if the patient is clinically unstable during after trauma. the acute phase and the MR imaging is not able to be obtained at The second limitation of our study could be correct identifi- an earlier stage. It could also be helpful in predicting neurologic cation and diagnosis of ligament disruption. T2-weighted images outcome in these cases. have shown moderate to high sensitivity with low specificity when compared with intraoperative findings in ligament disrup- CONCLUSIONS tion.23,24 Other sequences have been described in the literature We have presented the first study that correlates ALL, PLL, LF, that rule out soft-tissue injuries, such as STIR. One study showed and disk lesions according to the degree of spinal cord damage. a high correlation between STIR sequences and intraoperative Patients who had disruption of the LF showed greater length of findings in detecting soft-tissue injury.27 Unfortunately, the STIR lesion as measured by MR imaging. Additionally, the statistical sequence was not included in all cervical trauma protocols during association between number of ligaments injured and greater sig- the initial years of this study; in this sense, not all patients were nal changes in T2-weighted images of the spinal cord has been observed for STIR sequence, even though most were. We used demonstrated. STIR for assessment of soft tissue when it was available. Any as- We still have several concerns (timing of imaging, poor spec- sessment of the extent of damage in spinal cord and ligament ificity in measurement method, short follow-up period, lack of injuries is subjective, which poses another potential limitation objectivity); however, findings suggest that the extent of the T2 and source of bias. signal (after cervical spine trauma) correlates to a specific pattern Third, this study comprised a select group of cases that were of ligamentous injury. This might help determine neurologic out- managed in the intensive care or neurosurgery units. Minor cer- come when MR imaging is performed after the acute phase, in vical trauma with a lesser degree of lesion does not require MR that other features have less predictive potential. imaging by protocol in most cases. Furthermore, this study does Carefully designed studies, including neurologic outcome at not include all patients with cervical spine trauma, but it does follow-up, are needed to confirm some of our preliminary involve most patients with more severe cervical trauma. observations. Fourth, steroids were not included in our treatment protocol after Bracken et al40 could not corroborate statistically significant Disclosures: Ana Ramos—UNRELATED: Grants/Grants Pending: FIS* (*money paid to institution). benefits from steroids. Most patients did not receive steroids, and it was therefore not possible to access this information in relation REFERENCES to the time of imaging; thus, this factor could not be adequately 1. Hasler RM, Exadaktylos AK, Bouamra O, et al. Epidemiology and analyzed because it could have affected length of abnormal cord predictors of spinal injury in adult major trauma patients: Euro- signals. pean cohort study. Eur Spine J 2011;20:2174–80 Finally, lesion length represents the degree of SCI but is not a 2. Milby AH, Halpern CH, Guo W, et al. Prevalence of cervical spinal measure of neurologic outcome at follow-up. In this light, inter- injury in trauma. Neurosurg Focus 2008;25:E10 3. Bozzo A, Marcoux J, Radhakrishna M, et al. The role of magnetic pretation of these results should be taken with caution. Neverthe- resonance imaging in the management of acute spinal cord injury. less, initial neurologic examination tends to have a certain degree J Neurotrauma 2011;28:1401–11 of subjectivity: in patients with trauma, sedation, distractive pain, 4. Boldin C, Raith J, Fankhauser F, et al. Predicting neurologic recovery or clinical condition confounds reliable interpretation of the neu- in cervical spinal cord injury with postoperative MR imaging. Spine rologic state at admission. This is often the case when it is neces- 2006;31:554–59 5. Pizones J, Izquierdo E, Sanchez-Mariscal F, et al. Sequential damage sary to differentiate between ASIA A (complete SCI) and ASIA B assessment of the different components of the posterior ligamen- (incomplete, but no motor function preserved) in sedated pa- tous complex after magnetic resonance imaging interpretation: tients. In the acute phase, lesion length is a measure that has been prospective study 74 traumatic fractures. Spine 2012;37:E662–67 well correlated with neurologic recovery.9,11 Reliability issues, as 6. Song KJ, Kim GH, Lee KB. The efficacy of the modified classification system of soft tissue injury in extension injury of the lower cervical the result of feasibility of clinical examination for initial assess- spine. Spine 2008;33:E488–93 ment of cervical spine trauma, were better determined in our 7. Vaccaro AR, Madigan L, Schweitzer ME, et al. Magnetic resonance study when MRI was performed within 96 hours after trauma. We imaging analysis of soft tissue disruption after flexion-distraction prefer to use a continuous quantitative variable to indirectly ap- injuries of the subaxial cervical spine. Spine 2001;26:1866–72 praise the degree of SCI. Our results correlate with those of pre- 8. Flanders AE, Spettell CM, Tartaglino LM, et al. Forecasting motor recovery after cervical spinal cord injury: value of MR imaging. Ra- vious works,8,9,36 and larger lesions statistically correlate with diology 1996;201:649–55 more severe neurologic deficits with complete SCI in the acute 9. Miyanji F, Furlan JC, Aarabi B, et al. Acute cervical traumatic spinal phase (P Ͻ .001). However, other investigators have found that cord injury: MR imaging findings correlated with neurologic lesion length depends on the time of MR imaging after trauma.11 outcome: prospective study with 100 consecutive patients. Radiol- The value of the extent of the lesion may be overestimated in ogy 2007;243:820–27 10. Bondurant FJ, Cotler HB, Kulkarni MV, et al. Acute spinal cord patients for whom MR imaging was performed later. Therefore, injury: a study using physical examination and magnetic resonance we must determine which soft-tissue injury is associated with a imaging. Spine 1990;15:161–68 greater degree of SCI, given that this is a static finding; however, 11. Leypold BG, Flanders AE, Burns AS. The early evolution of spinal AJNR Am J Neuroradiol 35:1029–34 May 2014 www.ajnr.org 1033 cord lesions on MR imaging following traumatic spinal cord injury. resonance imaging for detecting posterior ligamentous complex in- AJNR Am J Neuroradiol 2008;29:1012–16 jury associated with thoracic and lumbar fractures. J Neurosurg 12. Andreoli C, Colaiacomo MC, Rojas Beccaglia M, et al. MRI in the 2003;99:20–26 acute phase of spinal cord traumatic lesions: relationship between 27. Lee HM, Kim HS, Kim DJ, et al. Reliability of magnetic resonance MRI findings and neurological outcome. Radiol Med 2005;110: imaging in detecting posterior ligament complex injury in thoraco- 636–45 lumbar spinal fractures. Spine 2000;25:2079–84 13. Ramon S, Dominguez R, Ramirez L, et al. Clinical and magnetic 28. Vaccaro AR, Hulbert RJ, Patel AA, et al. The subaxial cervical spine resonance imaging correlation in acute spinal cord injury. Spinal injury classification system: a novel approach to recognize the im- Cord 1997;35:664–73 portance of morphology, neurology, and integrity of the disco-lig- 14. Shimada K, Tokioka T. Sequential MR studies of cervical cord amentous complex. Spine 2007;32:2365–74 injury: correlation with neurological damage and clinical outcome. 29. Collignon F, Martin D, Lenelle J, et al. Acute traumatic central cord Spinal Cord 1999;37:410–15 syndrome: magnetic resonance imaging and clinical observations. 15. Flanders AE, Schaefer DM, Doan HT, et al. Acute cervical spine J Neurosurg 2002;96:29–33 trauma: correlation of MR imaging findings with degree of neuro- 30. Liao CC, Lui TN, Chen LR, et al. Spinal cord injury without radio- logic deficit. Radiology 1990;177:25–33 logical abnormality in preschool-aged children: correlation of 16. Kulkarni MV, Bondurant FJ, Rose SL, et al. 1.5 Tesla magnetic reso- magnetic resonance imaging findings with neurological outcomes. nance imaging of acute spinal trauma. Radiographics 1988;8: J Neurosurg 2005;103:17–23 1059–82 31. Silberstein M, Hennessy O. Implications of focal spinal cord lesions 17. Flanders AE, Spettell CM, Friedman DP, et al. The relationship be- following trauma: evaluation with magnetic resonance imaging. tween the functional abilities of patients with cervical spinal cord Paraplegia 1993;31:160–67 injury and the severity of damage revealed by MR imaging. AJNR 32. Yamashita Y, Takahashi M, Matsuno Y, et al. Acute spinal cord Am J Neuroradiol 1999;20:926–34 injury: magnetic resonance imaging correlated with myelopathy. 18. Alday R, Lobato, RD, Gomez PA. Cervical spine fractures. In: Neu- Br J Radiol 1991;64:201–09 rosurgery. New York: Churchill Livingstone; 1996 33. Dare AO, Dias MS, Li V. Magnetic resonance imaging correlation in 19. Pizones J, Sanchez-Mariscal F, Zuniga L, et al. Prospective analysis of pediatric spinal cord injury without radiographic abnormality. magnetic resonance imaging accuracy in diagnosing traumatic in- J Neurosurg 2002;97:33–39 juries of the posterior ligamentous complex of the thoracolumbar 34. Miranda P, Gomez P, Alday R, et al. Brown-Sequard syndrome after spine. Spine 2013;38:745–51 blunt cervical spine trauma: clinical and radiological correlations. 20. Pizones J, Zuniga L, Sanchez-Mariscal F, et al. MRI study of post- traumatic incompetence of posterior ligamentous complex: impor- Eur Spine J 2007;16:1165–70 tance of the supraspinous ligament. prospective study of 74 trau- 35. Dai L, Jia L. Central cord injury complicating acute cervical disc matic fractures. Eur Spine J 2012;21:2222–31 herniation in trauma. Spine 2000;25:331–35 21. Radcliff K, Su BW, Kepler CK, et al. Correlation of posterior liga- 36. Marciello MA, Flanders AE, Herbison GJ, et al. Magnetic resonance mentous complex injury and neurological injury to loss of vertebral imaging related to neurologic outcome in cervical spinal cord in- body height, kyphosis, and canal compromise. Spine 2012;37: jury. Arch Phys Med Rehabil 1993;74:940–46 1142–50 37. Selden NR, Quint DJ, Patel N, et al. Emergency magnetic resonance 22. Samartzis D, Wein SM, Shen FH, et al. A revisitation of distractive- imaging of cervical spinal cord injuries: clinical correlation and extension injuries of the subaxial cervical spine: a cadaveric and prognosis. Neurosurgery 1999;44:785–92 radiographic soft tissue analysis. Spine 2010;35:395–402 38. Shepard MJ, Bracken MB. Magnetic resonance imaging and neuro- 23. Goradia D, Linnau KF, Cohen WA, et al. Correlation of MR imaging logical recovery in acute spinal cord injury: observations from the findings with intraoperative findings after cervical spine trauma. National Acute Spinal Cord Injury Study 3. Spinal Cord 1999; AJNR Am J Neuroradiol 2007;28:209–15 37:833–37 24. Rihn JA, Fisher C, Harrop J, et al. Assessment of the posterior liga- 39. Miranda P, Gomez P, Alday R. Acute traumatic central cord mentous complex following acute cervical spine trauma. J Bone syndrome: analysis of clinical and radiological correlations. J Neu- Joint Surg Am 2010;92:583–89 rosurg Sci 2008;52:107–12 25. Carrino JA, Manton GL, Morrison WB, et al. Posterior longitudinal 40. Bracken MB, Shepard MJ, Collins WF, et al. A randomized, con- ligament status in cervical spine bilateral facet dislocations. Skeletal trolled trial of methylprednisolone or naloxone in the treatment of Radiol 2006;35:510–14 acute spinal-cord injury: results of the Second National Acute Spi- 26. Haba H, Taneichi H, Kotani Y, et al. Diagnostic accuracy of magnetic nal Cord Injury Study. N Engl J Med 1990;322:1405–11

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